The mammalian testis is innervated by extrinsic catecholaminergic nerves and responds to catecholamines with steroid secretion. Although the primate testis has also been shown to be innervated, potential differences in the density of this innervation between immature and sexually developed individuals have not been described. A recent study demonstrated that the primate ovary contains a network of neuron-like cells, and that some of these cells are catecholaminergic. It is thus possible that the male gonad is also endowed with a similar intragonadal source of catecholamines. In the present study we addressed these two issues. Catecholaminergic nerves were identified as such by their content of immunoreactive tyrosine hydroxylase (TH, the rate-limiting step in catecholamine biosynthesis), and in some cases by glyoxylic acid histochemistry. TH-containing fibers were abundant in testes from juvenile animals (1-2 yr of postnatal life), but the density of this innervation appeared to be reduced in adult animals, whose testis showed only a few TH-positive fibers scattered in the interstitial tissue. Testicular norepinephrine (NE) concentration was much lower in adult than in juvenile animals, suggesting that the marked increase in testicular weight that occurs with the attainment of sexual maturity is not accompanied by corresponding changes in NE content. At the ultrastructural level, testicular nerve fibers contained pleiomorphic, dense-core and clear vesicles, suggesting the presence of catecholamines and other neurotransmitters. In addition to this extrinsic catecholaminergic innervation, prepubertal testes, but not adult gonads, were found to contain an intrinsic population of TH-immunopositive neuron-like elements, identified as cells by confocal scanning laser microscopy. To determine if the prepubertal monkey testis indeed expresses the TH gene, testicular RNA was subjected to reverse transcription-PCR to amplify the 5'-end of TH mRNA, which encodes the regulatory domain of the enzyme. The cDNA obtained predicts an amino acid sequence similar, but not identical, to that encoded by the alternatively spliced type 1 TH mRNA form present in the adrenal gland. These results indicate that a) the primate testis receives a dual catecholaminergic input, one provided by the extrinsic innervation, and the other by neuron-like cells located within the gonad itself, and b) both sources are endowed with a high degree of phenotypical plasticity as they are prominent during the prepubertal period, and regress in adulthood. The presence in the testis of a TH mRNA variant encoding amino acid substitutions in its 5'-end suggests that regulation of testicular TH enzyme activity may include a gonad-specific component. A report of these findings has been submitted for publication.